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Regeneration of the flatworm Prosthiostomum siphunculus (Polycladida, Platyhelminthes).

ABSTRACT: Fueled by the discovery of head regeneration in triclads (planarians) two and a half centuries ago, flatworms have been the focus of regeneration research. But not all flatworms can regenerate equally well and to obtain a better picture of the characteristics and evolution of regeneration in flatworms other than planarians, the regeneration capacity and stem cell dynamics during regeneration in the flatworm order Polycladida are studied. Here, we show that as long as the brain remained at least partially intact, the polyclad Prosthiostomum siphunculus was able to regenerate submarginal eyes, cerebral eyes, pharynx, intestine and sucker. In the complete absence of the brain only wound closure was observed but no regeneration of missing organs. Amputated parts of the brain could not be regenerated. The overall regeneration capacity of P. siphunculus is a good fit for category III after a recently established system, in which most polyclads are currently classified. Intact animals showed proliferating cells in front of the brain which is an exception compared with most of the other free-living flatworms that have been observed so far. Proliferating cells could be found within the regeneration blastema, similar to all other flatworm taxa except triclads. No proliferation was observed in epidermis and pharynx. In pulse-chase experiments, the chased cells were found in all regenerated tissues and thereby shown to differentiate and migrate to replace the structures lost upon amputation.

SUBMITTER: Schadt T

PROVIDER: S-EPMC7960593 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BACKGROUND:Proseriates (Proseriata, Platyhelminthes) are free-living, mostly marine, flatworms measuring at most a few millimetres. In common with many flatworms, they are known to be capable of regeneration; however, few studies have been done on the details of regeneration in proseriates, and none cover cellular dynamics. We have tested the regeneration capacity of the proseriate Monocelis sp. by pre-pharyngeal amputation and provide the first comprehensive picture of the F-actin musculature, serotonergic nervous system and proliferating cells (S-phase in pulse and pulse-chase experiments and mitoses) in control animals and in regenerates. RESULTS:F-actin staining revealed a strong body wall, pharynx and dorsoventral musculature, while labelling of the serotonergic nervous system showed an orthogonal pattern and a well developed subepidermal plexus. Proliferating cells were distributed in two broad lateral bands along the anteroposterior axis and their anterior extension was delimited by the brain. No proliferating cells were detected in the pharynx or epidermis. Monocelis sp. was able to regenerate the pharynx and adhesive organs at the tip of the tail plate within 2 or 3 days of amputation, and genital organs within 8 to 10 days. Posterior pieces were not able to regenerate a head. The posterior regeneration blastema was found to be a centre of cell proliferation, whereas within the pharynx primordium, little or no proliferation was detected. The pharynx regenerated outside of the blastema and was largely, but not solely formed by cells that were proliferating at the time of amputation. CONCLUSIONS:Our findings suggest that proliferating cells or their offspring migrated to the place of organ differentiation and then stopped proliferating at that site. This mode of rebuilding organs resembles the mode of regeneration of the genital organs in another flatworm, Macrostomum lignano. Pharynx regeneration resembles embryonic development in Monocelis fusca and hints at the vertically directed pharynx being plesiomorphic in proseriates. Proliferation within the regeneration blastema has been detected in anterior and posterior blastemas of other flatworms, but is notably missing in triclads. The phylogenetic relationships of the flatworms studied indicate that proliferation within the blastema is the plesiomorphic condition in Platyhelminthes.

Dataset Information

Regeneration of the flatworm Prosthiostomum siphunculus (Polycladida, Platyhelminthes).

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